A mechanosensing mechanism controls plasma membrane shape homeostasis at the nanoscale
As cells migrate and experience forces from their surroundings, they constantly undergo mechanical deformations which reshape their plasma membrane (PM). To maintain homeostasis, cells need to detect and restore such changes, not only in terms of overall PM area and tension as previously described,...
| Main Authors: | , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2023-09-01
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| Series: | eLife |
| Subjects: | |
| Online Access: | https://elifesciences.org/articles/72316 |
| _version_ | 1797661015010181120 |
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| author | Xarxa Quiroga Nikhil Walani Andrea Disanza Albert Chavero Alexandra Mittens Francesc Tebar Xavier Trepat Robert G Parton María Isabel Geli Giorgio Scita Marino Arroyo Anabel-Lise Le Roux Pere Roca-Cusachs |
| author_facet | Xarxa Quiroga Nikhil Walani Andrea Disanza Albert Chavero Alexandra Mittens Francesc Tebar Xavier Trepat Robert G Parton María Isabel Geli Giorgio Scita Marino Arroyo Anabel-Lise Le Roux Pere Roca-Cusachs |
| author_sort | Xarxa Quiroga |
| collection | DOAJ |
| description | As cells migrate and experience forces from their surroundings, they constantly undergo mechanical deformations which reshape their plasma membrane (PM). To maintain homeostasis, cells need to detect and restore such changes, not only in terms of overall PM area and tension as previously described, but also in terms of local, nanoscale topography. Here, we describe a novel phenomenon, by which cells sense and restore mechanically induced PM nanoscale deformations. We show that cell stretch and subsequent compression reshape the PM in a way that generates local membrane evaginations in the 100 nm scale. These evaginations are recognized by I-BAR proteins, which triggers a burst of actin polymerization mediated by Rac1 and Arp2/3. The actin polymerization burst subsequently re-flattens the evagination, completing the mechanochemical feedback loop. Our results demonstrate a new mechanosensing mechanism for PM shape homeostasis, with potential applicability in different physiological scenarios. |
| first_indexed | 2024-03-11T18:39:16Z |
| format | Article |
| id | doaj.art-e420404ec4474c4ba1e511bee981ae9a |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-03-11T18:39:16Z |
| publishDate | 2023-09-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-e420404ec4474c4ba1e511bee981ae9a2023-10-12T13:51:04ZengeLife Sciences Publications LtdeLife2050-084X2023-09-011210.7554/eLife.72316A mechanosensing mechanism controls plasma membrane shape homeostasis at the nanoscaleXarxa Quiroga0Nikhil Walani1https://orcid.org/0000-0002-5248-9181Andrea Disanza2Albert Chavero3Alexandra Mittens4Francesc Tebar5Xavier Trepat6https://orcid.org/0000-0002-7621-5214Robert G Parton7https://orcid.org/0000-0002-7494-5248María Isabel Geli8https://orcid.org/0000-0002-3452-6700Giorgio Scita9https://orcid.org/0000-0001-7984-1889Marino Arroyo10Anabel-Lise Le Roux11https://orcid.org/0000-0003-4152-5658Pere Roca-Cusachs12https://orcid.org/0000-0001-6947-961XInstitute for Bioengineering of Catalonia, the Barcelona Institute of Technology (BIST), Barcelona, Spain; Departament de Biomedicina, Unitat de Biofísica i Bioenginyeria, Facultat de Medicina i Ciències de la Salut, Universitat de Barcelona, Barcelona, SpainDepartment of Applied Mechanics, IIT Delhi, New Delhi, IndiaIFOM ETS - The AIRC Institute of Molecular Oncology, Milan, ItalyDepartament de Biomedicina, Unitat de Biologia Cel·lular, Facultat de Medicina i Ciències de la Salut, Centre de Recerca Biomèdica CELLEX, Institut d’Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Universitat de Barcelona, Barcelona, SpainInstitute for Bioengineering of Catalonia, the Barcelona Institute of Technology (BIST), Barcelona, SpainDepartament de Biomedicina, Unitat de Biologia Cel·lular, Facultat de Medicina i Ciències de la Salut, Centre de Recerca Biomèdica CELLEX, Institut d’Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Universitat de Barcelona, Barcelona, SpainInstitute for Bioengineering of Catalonia, the Barcelona Institute of Technology (BIST), Barcelona, SpainInstitute for Molecular Bioscience and Centre for Microscopy and Microanalysis, University of Queensland, Brisbane, AustraliaInstitute for Molecular Biology of Barcelona (CSIC), Barcelona, SpainIFOM ETS - The AIRC Institute of Molecular Oncology, Milan, Italy; Department of Oncology and Haemato-Oncology, University of Milan, Milan, ItalyInstitute for Bioengineering of Catalonia, the Barcelona Institute of Technology (BIST), Barcelona, Spain; Universitat Politècnica de Catalunya (UPC), Campus Nord, Carrer de Jordi Girona, Barcelona, Spain; Centre Internacional de Mètodes Numèrics en Enginyeria (CIMNE), Barcelona, SpainInstitute for Bioengineering of Catalonia, the Barcelona Institute of Technology (BIST), Barcelona, SpainInstitute for Bioengineering of Catalonia, the Barcelona Institute of Technology (BIST), Barcelona, Spain; Departament de Biomedicina, Unitat de Biofísica i Bioenginyeria, Facultat de Medicina i Ciències de la Salut, Universitat de Barcelona, Barcelona, SpainAs cells migrate and experience forces from their surroundings, they constantly undergo mechanical deformations which reshape their plasma membrane (PM). To maintain homeostasis, cells need to detect and restore such changes, not only in terms of overall PM area and tension as previously described, but also in terms of local, nanoscale topography. Here, we describe a novel phenomenon, by which cells sense and restore mechanically induced PM nanoscale deformations. We show that cell stretch and subsequent compression reshape the PM in a way that generates local membrane evaginations in the 100 nm scale. These evaginations are recognized by I-BAR proteins, which triggers a burst of actin polymerization mediated by Rac1 and Arp2/3. The actin polymerization burst subsequently re-flattens the evagination, completing the mechanochemical feedback loop. Our results demonstrate a new mechanosensing mechanism for PM shape homeostasis, with potential applicability in different physiological scenarios.https://elifesciences.org/articles/72316mechanobiologybar proteinsmembrane biophysics |
| spellingShingle | Xarxa Quiroga Nikhil Walani Andrea Disanza Albert Chavero Alexandra Mittens Francesc Tebar Xavier Trepat Robert G Parton María Isabel Geli Giorgio Scita Marino Arroyo Anabel-Lise Le Roux Pere Roca-Cusachs A mechanosensing mechanism controls plasma membrane shape homeostasis at the nanoscale eLife mechanobiology bar proteins membrane biophysics |
| title | A mechanosensing mechanism controls plasma membrane shape homeostasis at the nanoscale |
| title_full | A mechanosensing mechanism controls plasma membrane shape homeostasis at the nanoscale |
| title_fullStr | A mechanosensing mechanism controls plasma membrane shape homeostasis at the nanoscale |
| title_full_unstemmed | A mechanosensing mechanism controls plasma membrane shape homeostasis at the nanoscale |
| title_short | A mechanosensing mechanism controls plasma membrane shape homeostasis at the nanoscale |
| title_sort | mechanosensing mechanism controls plasma membrane shape homeostasis at the nanoscale |
| topic | mechanobiology bar proteins membrane biophysics |
| url | https://elifesciences.org/articles/72316 |
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